Elsevier

Chemosphere

Volume 301, August 2022, 134698
Chemosphere

Exposure to ambient air pollution and osteoarthritis; an animal study

https://doi.org/10.1016/j.chemosphere.2022.134698Get rights and content

Highlights

  • The effect of exposure to air pollution and OA was assessed based on an animal model.

  • The OA biomarkers, i.e., osteocalcin, COMP, NTX-I and cytokines, were measured in the blood plasma.

  • The osteocalcin was significantly lower in PM and PM-gaseous exposure groups compared to control.

  • Compared to the control, COMP and NTX-I were increased significantly in the PMs and PMs-gaseous exposure groups.

  • Exposure to PM and gaseous pollutants significantly increased plasma cytokine levels compared to control.

Abstract

Exposure to air pollution has been associated with many adverse health effects. However, the evidence on the effects on osteoarthritis (OA) is scarce and the potential mechanism is unclear yet. Therefore, this study assessed the effect of exposure to air pollution (gaseous and particulate matter) and OA based on an animal model. We used four groups of female rats, including i) exposure to PMs and gaseous pollutants, ii) exposure only to gaseous pollutants, iii) exposure only to PMs, and iv) control (unexposed) group. The OA biomarkers, i.e., osteocalcin, cartilage oligomeric protein (COMP), and N-Telopeptides of Type I Collagen (NTX-I) and cytokines were measured in the plasma to detect the effect of exposure to ambient air pollution on OA in this animal model. The forced jogging exercises for 1 h and 5 days per week were used to record the physical activities. The median (interquartile range) concentrations of PM2.5 and PM10 were 35.9 (15.4) and 47.5 (22.5) μg/m3, respectively. The median (interquartile range (IQR)) of PM2.5, PM10, CO, NO2, SO2 and O3 in the inlet ambient air were 36.9 (16.9), 51.7 (23.6) μg/m3, 16.1 (12.5) ppm, 413.7 (177.1), 334.2 (218.8) and 208.9 (113.1) ppb, respectively. The osteocalcin was significantly lower in PM as well as PM-gaseous exposure groups compared to control. Moreover, expressions of COMP were increased significantly in the PMs and exposure group compared to the control. For the PMs-gaseous exposure group, the COMP expressions were the highest compared to the control group. Similar results were observed for NTX-I. Exposure to PM and gaseous pollutants significantly increased plasma cytokine levels compared to control. Overall, our study showed a significant effect of exposure to PMs and PMs-gaseous exposure with OA in rats. Moreover, we observed a synergistic effect of mixed gaseous-PMs exposure compared to PMs and gaseous pollutants separately.

Introduction

Ambient air pollution including gaseous (e.g., carbon monoxide (CO), ozone (O3), nitrogen oxides (NOx), sulfur dioxide (SO2), etc.) and particulate matter (PM) pollutants with different size fractions (i.e., PM2.5 and PM10) have been suggested as a major problem in urban areas (Nikoonahad et al., 2017; Ghaffari et al., 2017). Transportation, industrial activities and household biomass burning are the main sources of air pollution in urban areas (Gholizadeh et al., 2019; Mohammadi et al., 2020; Abdolahnejad et al., 2018; Campbell- Lendrum and Pr ü ss-Ust ü n, 2019). The available evidence reported that indoor and outdoor exposure to air pollution was associated with different adverse health outcomes, including excess mortality, respiratory and cardiovascular diseases, diabetes type 2, neuropsychological problems, adverse birth outcomes, risk of osteoporosis and bone fractures and rheumatoid arthritis (Mohammadi et al., 2019; Franklin et al., 2015; Burki, 2021; Kim et al., 2018; Nguyen, 2018; Shin et al., 2019a). On the other hand, physical activities (e.g., running and walking daily) are suggested as non-pharmacological methods to improve the quality of life and human health (Vina et al., 2012; Yang, 2019). However, it can lead to higher exposure to air pollution, especially in urban areas with air quality exceeding the world health organization (WHO) guideline (Tainio et al., 2021). According to the last report of WHO in 2019, more than 90% of the global population lived in areas with air quality poorer than WHO guidelines in 2005, and with decrease in the WHO guideline values in 2021, this percentage increased (Burki, 2021). Therefore, increased outdoor physical activities in these areas may increase adverse health effects (e.g., Osteoarthritis (OA)) related to exposure to high levels of air pollution (Kulkarni et al., 2020).

Osteoarthritis (OA) is a progressive degenerative joint disease that occurs due to synovium, cartilage, and subchondral bone damage (Li et al., 2013; Loeser et al., 2012). Symptoms of OA appear from the middle age period, and it has been reported that the prevalence of OA was related to several factors, e.g., age, obesity, gender, occupation, and physical and sports activities (Heidari, 2011; Palazzo et al., 2016; Plotnikoff et al., 2015). Moreover, cytokines, e.g., TNF-α, IL-1b in the membrane and synovial fluid, cartilage of the patients, and subchondral bone, are suggested as biomarkers of OA (Wang and He, 2018; Stannus et al., 2010; Shetty et al., 2021).

An emerging body of evidence has reported that outdoor physical activities in polluted areas significantly increase air pollution intake (Tainio et al., 2021). Nevertheless, the influence of exposure to air pollution on OA in the knee joint is unclear yet. The experimental animal model studies based on mice, rats, and other rodents have been used to study the underlying mechanism of respiratory and cardiovascular diseases related to air pollutants due to various benefits, e.g., low cost, high quality, and availability (Shang and Sun, 2018; Poojary et al., 2020; Gupta et al., 2021; Zhu et al., 2021; Sengodan and Appusamy, 2020; Margiana et al., 2018). However, the available evidence on the effect of exposure to air pollution on OA is very scarce (Peng et al., 2019). A previous animal model study assessed only the influence of single high dose PM exposure on knee joint OA development or severity (Peng et al., 2019). However, in the present study, for the first time, we aimed to assess the effect of exposure to gaseous pollutants (SO2, NO2, O3, and CO) as well as PM (PM2.5 and PM10) separately and together on OA that can cover the synergistic effects of exposure to a mixture of air pollutants based on an animal model study.

Section snippets

Animals

We used Wistar rat female rats aged 10 weeks old and weighing 400 to 500 gr. The rats were housed in a room with controlled temperature (20–25 C), humidity (40–60%) and a 12 h light/dark cycle. The rats were held for 48 h before experiments under specific pathogen-free access to enough food and water ad libitum. Our animal model study was approved by the ethic committee of Universitas Nahdlatul Wathan Mataram.

Study design and exposure assessment

The animal pilots were located in Universitas Nahdlatul Wathan Mataram. The female

Ambient air pollution concentrations

The median (interquartile range (IQR)) of PM2.5, PM10, CO, NO2, SO2 and O3 in the inlet ambient air for EPG group were 36.9 (16.9), 51.7 (23.6) μg/m3, 16.1 (12.5) ppm, 413.7 (177.1), 334.2 (218.8) and 208.9 (113.1) ppb, respectively (Fig. 1). The concentration of these pollutants in EG and EP groups was similar to the EPG. The medina (IQR) of PM2.5, PM10, CO, NO2, SO2 and O3 in concentrations for control group were 3.5 (1.2), 8.4 (2.4) μg/m3, 1.7 (0.5) ppm, 25.7 (15.6), 14.9 (12.4), 17.7 (11.2)

Discussion

To the best of our knowledge, this is the first animal study that investigated the effect of exposure to the mixture of ambient gaseous and PM pollutants on OA. We found that exposure to PM and a mix of PM-gaseous pollutants significantly increased COMP and NTX-I and decreased osteocalcin in rats, which was stronger for the PM-gaseous exposure group. Moreover, exposure to ambient air pollution significantly increased cytokines in blood plasma compared control group. The highest mean difference

Conclusion

Our animal studies showed a causal link between exposure to air pollution during physical activity and OA in rats. Exposure to PM and a mixture of PM and gaseous pollutants increased plasma levels of COMP and NTX-I and decreased osteocalcin compared to control. The cytokines were increased significantly in all exposure groups compared to the control. A synergistic effect was observed for the EPG group compared EP and EG group. Our study indicated that OA-related exposure to air pollution might

Credit author statement

Abyadul Fitriyah: Conceptualization, Methodology, Software, Writing – original draft preparation. Denis Andreevich Nikolenko: Data curation, Writing – original draft preparation. Walid Kamal Abdelbasset: Visualization, Investigation. Marwah Suliman Maashi: Visualization, Investigation., Abduladheem Turki Jalil: Visualization, Investigation., Ghulam Yasin: Visualization, Investigation., Mohammed Mustafa Abdulkadhm: Visualization, Investigation., G.U. Samieva: Visualization, Investigation. Holya

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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